Empirical and model-based evidence for a negligible role of cattle in peste des petits ruminants virus transmission and eradication.


Journal

Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179

Informations de publication

Date de publication:
03 Aug 2024
Historique:
received: 12 05 2023
accepted: 23 07 2024
medline: 3 8 2024
pubmed: 3 8 2024
entrez: 2 8 2024
Statut: epublish

Résumé

Peste des petits ruminants virus (PPRV) is a multi-host pathogen with sheep and goats as main hosts. To investigate the role of cattle in the epidemiology of PPR, we simulated conditions similar to East African zero-grazing husbandry practices in a series of trials with local Zebu cattle (Bos taurus indicus) co-housed with goats (Capra aegagrus hircus). Furthermore, we developed a mathematical model to assess the impact of PPRV-transmission from cattle to goats. Of the 32 cattle intranasally infected with the locally endemic lineage IV strain PPRV/Ethiopia/Habru/2014 none transmitted PPRV to 32 co-housed goats. However, these cattle or cattle co-housed with PPRV-infected goats seroconverted. The results confirm previous studies that cattle currently play a negligible role in PPRV-transmission and small ruminant vaccination is sufficient for eradication. However, the possible emergence of PPRV strains more virulent for cattle may impact eradication. Therefore, continued monitoring of PPRV circulation and evolution is recommended.

Identifiants

pubmed: 39095591
doi: 10.1038/s42003-024-06619-2
pii: 10.1038/s42003-024-06619-2
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

937

Subventions

Organisme : Bill and Melinda Gates Foundation (Bill & Melinda Gates Foundation)
ID : SEBI / ROSLIN 2340
Organisme : Bill and Melinda Gates Foundation (Bill & Melinda Gates Foundation)
ID : OPP1083453
Organisme : RCUK | Biotechnology and Biological Sciences Research Council (BBSRC)
ID : Grant BB/R004250/1
Organisme : Penn State | Huck Institutes of the Life Sciences (Huck Institutes)
ID : Distinguished Chair

Informations de copyright

© 2024. The Author(s).

Références

Portier, J. et al. Multi-host disease management: the why and the how to include wildlife. BMC Vet. Res. 15, 295 (2019).
pubmed: 31412882 pmcid: 6694651 doi: 10.1186/s12917-019-2030-6
Haydon, D. T. et al. Identifying reservoirs of infection: a conceptual and practical challenge. Emerg. Infect. Dis. 8, 1468–1473 (2002).
pubmed: 12498665 doi: 10.3201/eid0812.010317
Buhnerkempe, M. G. et al. Eight challenges in modelling disease ecology in multi-host, multi-agent systems. Epidemics 10, 26–30 (2015).
pubmed: 25843378 doi: 10.1016/j.epidem.2014.10.001
Lembo, T. et al. Exploring reservoir dynamics: a case study of rabies in the Serengeti ecosystem. J. Appl. Ecol. 45, 1246–1257 (2008).
pubmed: 22427710 pmcid: 3303133 doi: 10.1111/j.1365-2664.2008.01468.x
Mancy, R. et al. Rabies shows how scale of transmission can enable acute infections to persist at low prevalence. Science 376, 512–516 (2022).
pubmed: 35482879 pmcid: 7613728 doi: 10.1126/science.abn0713
Townsend, S. E. et al. Surveillance guidelines for disease elimination: a case study of canine rabies. Comp. Immunol. Microbiol. Infect. Dis. 36, 249–261 (2013).
pubmed: 23260376 pmcid: 3693035 doi: 10.1016/j.cimid.2012.10.008
Ferguson, E. A. et al. Heterogeneity in the spread and control of infectious disease: consequences for the elimination of canine rabies. Sci. Rep. 5, 1–13 (2015).
doi: 10.1038/srep18232
FAO. Global Strategy for the Control and Eradication of PPR. https://openknowledge.fao.org/handle/20.500.14283/i4460e (2015).
Baron, M. D., Diop, B., Njeumi, F., Willett, B. J. & Bailey, D. Future research to underpin successful peste des petits ruminants virus (PPRV) eradication. J. Gen. Virol. 98, 2635–2644 (2017).
pubmed: 29022862 pmcid: 5845661 doi: 10.1099/jgv.0.000944
WOAH. Global control and eradication of peste des petits ruminants. https://www.woah.org/app/uploads/2021/03/ppr-advocacy-en.pdf (2015).
Crosby, S. L., Cosby, S. L. & Crosby, S. L. Morbillivirus cross-species infection: is there a risk for humans? Future Virol. 7, 1103–1113 (2012).
doi: 10.2217/fvl.12.103
Hamdy, F. & Dardiri, A. Response of white-tailed deer to infection with peste des petits ruminants virus. J. Wildl. Dis. 12, 516–522 (1976).
pubmed: 16502689 doi: 10.7589/0090-3558-12.4.516
Schulz, C., Fast, C., Schlottau, K., Hoffmann, B. & Beer, M. Neglected hosts of small ruminant morbillivirus. Emerg. Infect. Dis. 24, 2334–2337 (2018).
pubmed: 30457523 pmcid: 6256395 doi: 10.3201/eid2412.180507
Nawathe, D. R. & Taylor, W. P. Experimental infection of domestic pigs with the virus of peste des petits ruminants. Trop. Anim. Health Prod. 11, 120–122 (1979).
pubmed: 462558 doi: 10.1007/BF02237785
Wernery, U. Peste des petits ruminants (PPR) in camelids with own investigation. J. Camel Pract. Res. 18, 219–223 (2011).
Fakri, F., Bamouh, Z., Jazouli, M. & Omari, K. Experimental infection of dromedary camels with virulent virus of Peste des Petits Ruminants. Vet. Microbiol. 235, 195–198 (2019).
pubmed: 31383302 doi: 10.1016/j.vetmic.2019.07.004
El-Hakim, U. A. The role of camels in dessimination of peste des petits ruminants virus among sheep and goats in Saudi Arabia. Assiut Vet. Med. J. 52, 132–145 (2006).
doi: 10.21608/avmj.2006.177390
Saeed, I. K. et al. A study on transmission of Peste des petits ruminants virus between dromedary camels and small ruminants. J. Infect. Dev. Ctries. 16, 374–382 (2022).
pubmed: 35298435 doi: 10.3855/jidc.14947
Balamurugan, V. et al. Seroprevalence of Peste des petits ruminants in cattle and buffaloes from Southern Peninsular India. Trop. Anim. Health Prod. 44, 301–306 (2012).
pubmed: 22105906 doi: 10.1007/s11250-011-0020-1
Khan, H. A. et al. The detection of antibody against peste des petits ruminants virus in sheep, goats, cattle and buffaloes. Trop. Anim. Health Prod. 40, 521–527 (2008).
pubmed: 18716909 doi: 10.1007/s11250-008-9129-2
Balamurugan, V. et al. Prevalence of Peste-des-petits-ruminant virus antibodies in cattle, buffaloes, sheep and goats in India. VirusDisease 25, 85–90 (2014).
pubmed: 24426314 doi: 10.1007/s13337-013-0177-5
Intisar, K. S. et al. Peste des petits ruminants infection in domestic ruminants in Sudan. Trop. Anim. Health Prod. 49, 747–754 (2017).
pubmed: 28321790 doi: 10.1007/s11250-017-1254-3
Ali, W. H. et al. Serological investigations of peste des petits ruminants among cattle in the Sudan. Trop. Anim. Health Prod. 51, 655–659 (2018).
pubmed: 30357603 doi: 10.1007/s11250-018-1740-2
Haroun, M., Hajer, I., Mukhtar, M. & Ali, B. E. Detection of antibodies against peste des petits ruminants virus in sera of cattle, camels, sheep and goats in Sudan. Vet. Res. Commun. 26, 537–541 (2002).
pubmed: 12416868 doi: 10.1023/A:1020239515020
Herzog, C. M. et al. Pastoral production is associated with increased peste des petits ruminants seroprevalence in northern Tanzania across sheep, goats and cattle. Epidemiol. Infect. 147, 1–9 (2019).
doi: 10.1017/S0950268819001262
Albayrak, H. & Gür, S. A serologic investigation for Peste des petits ruminants infection in sheep, cattle and camels (Camelus dromedarius) in Aydin province, West Anatolia. Trop. Anim. Health Prod. 42, 151–153 (2010).
pubmed: 19554466 doi: 10.1007/s11250-009-9400-1
Lembo, T. et al. Peste des petits ruminants infection among cattle and wildlife in northern Tanzania. Emerg. Infect. Dis. 19, 2037–2040 (2013).
pubmed: 24274684 pmcid: 3840886 doi: 10.3201/eid1912.130973
Abraham, G. et al. Antibody seroprevalences against peste des petits ruminants (PPR) virus in camels, cattle, goats and sheep in Ethiopia. Prev. Vet. Med. 70, 51–57 (2005).
pubmed: 15967242 doi: 10.1016/j.prevetmed.2005.02.011
Rashid, A., Asim, M. & Hussain, A. Seroprevalence of peste des petits ruminants (PPR) virus in goats, sheep, cattle, at Livestock Production Research Institute Bahadurnagar Okara. J. Anim. Pl Sci. 18, 114–116 (2008).
Sen, A. et al. Detection of subclinical peste des petits ruminants virus infection in experimental cattle. VirusDisease 25, 408–411 (2014).
pubmed: 25674614 pmcid: 4188194 doi: 10.1007/s13337-014-0213-0
Abubakar, M. et al. Serological detection of antibodies to peste des petits ruminants virus in large ruminants. Transbound. Emerg. Dis. 64, 513–519 (2017).
Ngangnou, A., Zoyem, N., Hamet, M. & Abdoulkadiri, S. Evaluation de la protection vaccinale contre la peste bovine au Cameroun III, Evaluation globale. Rev. Elev. Med. Vet. Pays Trop. 49, 18–22 (1996).
pubmed: 8881414 doi: 10.19182/remvt.9539
Tounkara, K. et al. Epidemiologie de la peste des petits ruminants (PPR) et de la peste bovine au Mali: enquetes serologiques. Rev. d’élevage Médecine v.étérinaire des. pays Trop. v.étérinaire des. pays Trop. 49, 273–277 (1996).
doi: 10.19182/remvt.9495
Couacy-Hymann, E. et al. Experimental infection of cattle with wild type peste-des-petits-ruminants virus – Their role in its maintenance and spread. Res. Vet. Sci. 124, 118–122 (2019).
pubmed: 30878633 doi: 10.1016/j.rvsc.2019.02.011
Schulz, C. et al. Camelids and cattle are dead-end hosts for Peste-des-petits-ruminants virus. Viruses 11, 1133 (2019).
pubmed: 31817946 pmcid: 6950723 doi: 10.3390/v11121133
Alemu, B. et al. Molecular detection and phylogenetic analysis of Peste des petits ruminants virus circulating in small ruminants in eastern Amhara region, Ethiopia. BMC Vet. Res. 15, 1–9 (2019).
doi: 10.1186/s12917-019-1828-6
Adombi, C. M. M. et al. Monkey CV1 cell line expressing the sheep-goat SLAM protein: A highly sensitive cell line for the isolation of peste des petits ruminants virus from pathological specimens. J. Virol. Methods 173, 306–313 (2011).
pubmed: 21371505 pmcid: 3166437 doi: 10.1016/j.jviromet.2011.02.024
von Messling, V., Springfeld, C., Devaux, P. & Cattaneo, R. A ferret model of canine distemper virus virulence and immunosuppression. J. Virol. 77, 12579–12591 (2003).
doi: 10.1128/JVI.77.23.12579-12591.2003
Hierholzer, J. C. & Killington, R. A. Virus isolation and quantitation. Virol. Methods Man. 25–46 https://doi.org/10.1016/b978-012465330-6/50003-8 (1996).
Pope, R. A. et al. Early events following experimental infection with Peste-Des-Petits ruminants virus suggest immune cell targeting. PLoS One 8, e55830 (2013).
pubmed: 23418464 pmcid: 3572172 doi: 10.1371/journal.pone.0055830
Libeau, G. et al. Development of competitive ELISA for the peste des petits ruminants virus using a recombinant nucleoprotein. Res. Vet. Sci. 58, 50–55 (1995).
pubmed: 7709061 doi: 10.1016/0034-5288(95)90088-8
Batten, C. A. et al. A real time RT-PCR assay for the specific detection of Peste des petits ruminants virus. J. Virol. Methods 171, 401–404 (2011).
pubmed: 21126540 doi: 10.1016/j.jviromet.2010.11.022
Johnson, A. A., Ott, M. Q. & Dogucu, M. The Beta-Binomial Bayesian Model. in Bayes Rules! An Introduction to Applied Bayesian Modeling (CRC Press, 2022).
Dogucu, M., Johnson, A. & Ott, M. bayesrules: Datasets and Supplemental Functions from Bayes Rules! https://github.com/bayes-rules/bayesrules (2021).
Fournié, G., Waret-Szkuta, A., Camacho, A., Yigezu, L. M. & Pfeiffer, D. U. A dynamic model of transmission and elimination of peste des petits ruminants in Ethiopia. Proc. Natl. Acad. Sci. USA 115, 8454–8459 (2018).
pubmed: 30054316 pmcid: 6099864 doi: 10.1073/pnas.1711646115
Diekmann, O., Heesterbeek, J. A. P. & Metz, J. A. J. On the definition and the computation of the basic reproduction ratio R0 in models for infectious diseases in heterogeneous populations. J. Math. Biol. 28, 365–382 (1990).
pubmed: 2117040 doi: 10.1007/BF00178324
Yitagesu, E. & Alemnew, E. Mortality rate of Boer, Central Highland goat and their crosses in Ethiopia: Nonparametric survival analysis and piecewise exponential model. Vet. Med. Sci. 8, 2183–2193 (2022).
pubmed: 35810464 pmcid: 9514490 doi: 10.1002/vms3.876
Logan, N. et al. Efficient generation of vesicular stomatitis virus (VSV)-pseudotypes bearing morbilliviral glycoproteins and their use in quantifying virus neutralising antibodies. Vaccine 34, 814–822 (2016).
pubmed: 26706278 pmcid: 4742518 doi: 10.1016/j.vaccine.2015.12.006
Wan, Y. et al. PPRV-induced autophagy facilitates infectious virus transmission by the exosomal pathway. J. Virol. 96, e0024422 (2022).
pubmed: 35319226 doi: 10.1128/jvi.00244-22
Abdullah, N. et al. Structure-guided identification of a non-human morbillivirus with zoonotic potential. J. Virol. 92, e01248 (2018).
pubmed: 30232185 pmcid: 6232486 doi: 10.1128/JVI.01248-18
Tirumurugaan, K. G. et al. RNAseq reveals the contribution of interferon stimulated genes to the increased host defense and decreased PPR viral replication in cattle. Viruses 12, 463 (2020).
pubmed: 32325933 pmcid: 7232496 doi: 10.3390/v12040463
Sawatsky, B., Cattaneo, R. & von Messling, V. Canine distemper virus spread and transmission to naive ferrets: selective pressure on signaling lymphocyte activation molecule-dependent entry. J. Virol. 92, 1–13 (2018).
doi: 10.1128/JVI.00669-18
Rume, V. N. et al. Molecular epidemiological update of Peste des Petits Ruminants virus (PPRV) in Ethiopia. Vet. Microbiol. 235, 229–233 (2019).
pubmed: 31383306 doi: 10.1016/j.vetmic.2019.07.006
Kwiatek, O. et al. Asian lineage of Peste des petits ruminants virus, Africa. Emerg. Infect. Dis. 17, 1223–1231 (2011).
pubmed: 21762576 pmcid: 3381390 doi: 10.3201/eid1707.101216
Rossiter, P., Wamwayi, H. & Ndungu, E. Rinderpest seroprevalence in wildlife in Kenya and Tanzania, 1982–1993. Prev. Vet. Med. 75, 1–7 (2006).
pubmed: 16529830 doi: 10.1016/j.prevetmed.2005.12.007
Lloyd-Smith, J. O. Vacated niches, competitive release and the community ecology of pathogen eradication. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 368, 1–12 (2013).
doi: 10.1098/rstb.2012.0150
Kennedy, J. M. et al. Canine and phocine distemper viruses: global spread and genetic basis of jumping species barriers. Viruses 11, 944 (2019).
pubmed: 31615092 pmcid: 6833027 doi: 10.3390/v11100944
Takeda, M., Seki, F., Yamamoto, Y., Nao, N. & Tokiwa, H. Animal morbilliviruses and their cross-species transmission potential. Curr. Opin. Virol. 41, 38–45 (2020).
pubmed: 32344228 doi: 10.1016/j.coviro.2020.03.005
Beineke, A., Baumgärtner, W. & Wohlsein, P. Cross-species transmission of canine distemper virus-an update. One Health 1, 49–59 (2015).
pubmed: 28616465 pmcid: 5462633 doi: 10.1016/j.onehlt.2015.09.002
Logan, N. et al. Enhanced immunosurveillance for animal morbilliviruses using vesicular stomatitis virus (VSV) pseudotypes. Vaccine 34, 5736–5743 (2016).
pubmed: 27742221 pmcid: 5084683 doi: 10.1016/j.vaccine.2016.10.010
Rimoin, A. W. et al. Major increase in human monkeypox incidence 30 years after smallpox vaccination campaigns cease in the Democratic Republic of Congo. Proc. Natl. Acad. Sci. USA 107, 16262–16267 (2010).
pubmed: 20805472 pmcid: 2941342 doi: 10.1073/pnas.1005769107
Damas, J. et al. Broad host range of SARS-CoV-2 predicted by comparative and structural analysis of ACE2 in vertebrates. Proc. Natl. Acad. Sci. USA 117, 22311–22322 (2020).
pubmed: 32826334 pmcid: 7486773 doi: 10.1073/pnas.2010146117
Chandler, J. C. et al. SARS-CoV-2 exposure in wild white-tailed deer (Odocoileus virginianus). Proc. Natl. Acad. Sci. USA 118, 1–3 (2021).
doi: 10.1073/pnas.2114828118
Oreshkova, N. et al. SARS-CoV-2 infection in farmed minks, the Netherlands, April and May 2020. Eurosurveillance 25, 1–7 (2020).
doi: 10.2807/1560-7917.ES.2020.25.23.2001005
Agüero, M. et al. Highly pathogenic avian influenza A(H5N1) virus infection in farmed minks, Spain, October 2022. Eurosurveillance 28, 2300001 (2023).
pubmed: 36695488 pmcid: 9853945 doi: 10.2807/1560-7917.ES.2023.28.3.2300001
Ohishi, K. et al. Recent host range expansion of canine distemper virus and variation in its receptor, the signaling lymphocyte activation molecule, in carnivores. J. Wildl. Dis. 50, 596–606 (2014).
pubmed: 24807184 doi: 10.7589/2013-09-228
Nikolin, V. M. et al. Canine distemper virus in the Serengeti ecosystem: molecular adaptation to different carnivore species. Mol. Ecol. 26, 2111–2130 (2017).
pubmed: 27928865 doi: 10.1111/mec.13902
Bieringer, M. et al. Experimental adaptation of wild-type canine distemper virus (CDV) to the human entry receptor CD150. PLoS One 8, 1–7 (2013).
doi: 10.1371/journal.pone.0057488
Plowright, W. & Mcculloch, B. Investigations on the incidence of rinderpest virus infection in game animals of N. Tanganyika and S. Kenya 1960–63. J. Hyg. (Lond.). 65, 343–358 (1967).
pubmed: 5233989 pmcid: 2130342 doi: 10.1017/S0022172400045861
Barrett, T. et al. Rediscovery of the second African lineage of rinderpest virus: Its epidemiological significance. Vet. Rec. 142, 669–671 (1998).
pubmed: 9670447 doi: 10.1136/vr.142.24.669
Mariner, J. C. & Roeder, P. L. Use of participatory epidemiology in studies of the persistence of lineage 2 rinderpest virus in East Africa. Vet. Rec. 152, 641–647 (2003).
pubmed: 12790233 doi: 10.1136/vr.152.21.641
Bataille, A. et al. Combining viral genetic and animal mobility network data to unravel peste des petits ruminants transmission dynamics in West Africa. PLoS Pathog. 17, 1–22 (2021).
doi: 10.1371/journal.ppat.1009397
GetDrawings.com. Goat Silhouette Icon. https://getdrawings.com/get-silhouette#show-goat-silhouette-14.jpg .
GetDrawings.com. Cattle Silhouette Icon. http://getdrawings.com/cattle-silhouette-clip-art#cattle-silhouette-clip-art-7.png .
Clker.com. Needle Icon. https://www.clker.com/clipart-722884.html .
ClipartsZone. Sheep Silhouette Icon. https://cliparts.zone/clipart/1544667 .

Auteurs

Catherine M Herzog (CM)

Center for Infectious Disease Dynamics, Pennsylvania State University, University Park, PA, USA. cqh5447@psu.edu.

Fasil Aklilu (F)

Animal Health Institute (AHI), Sebeta, Ethiopia.

Demeke Sibhatu (D)

Animal Health Institute (AHI), Sebeta, Ethiopia.

Dereje Shegu (D)

Animal Health Institute (AHI), Sebeta, Ethiopia.

Redeat Belaineh (R)

Animal Health Institute (AHI), Sebeta, Ethiopia.

Abde Aliy Mohammed (AA)

Animal Health Institute (AHI), Sebeta, Ethiopia.

Menbere Kidane (M)

Animal Health Institute (AHI), Sebeta, Ethiopia.

Claudia Schulz (C)

Institute of Virology, Department of Biological Sciences and Pathobiology, University of Veterinary Medicine Vienna, Vienna, Austria.

Brian J Willett (BJ)

MRC-University of Glasgow Centre for Virus Research, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK.

Sarah Cleaveland (S)

School of Biodiversity, One Health and Veterinary Medicine, College of Medical, Veterinary and Life Sciences, University of Glasgow, Glasgow, UK.

Dalan Bailey (D)

The Pirbright Institute, Pirbright, UK.

Andrew R Peters (AR)

Supporting Evidence Based Interventions (SEBI), University of Edinburgh, Edinburgh, UK.

Isabella M Cattadori (IM)

Center for Infectious Disease Dynamics, Pennsylvania State University, University Park, PA, USA.

Peter J Hudson (PJ)

Center for Infectious Disease Dynamics, Pennsylvania State University, University Park, PA, USA.

Hagos Asgedom (H)

Animal Health Institute (AHI), Sebeta, Ethiopia.

Joram Buza (J)

Nelson Mandela African Institute of Science and Technology, Arusha, Tanzania.

Mesfin Sahle Forza (MS)

Animal Health Institute (AHI), Sebeta, Ethiopia.

Tesfaye Rufael Chibssa (TR)

Animal Health Institute (AHI), Sebeta, Ethiopia.

Solomon Gebre (S)

Animal Health Institute (AHI), Sebeta, Ethiopia.

Nick Juleff (N)

Bill & Melinda Gates Foundation, Seattle, WA, USA.

Ottar N Bjørnstad (ON)

Center for Infectious Disease Dynamics, Pennsylvania State University, University Park, PA, USA.

Michael D Baron (MD)

The Pirbright Institute, Pirbright, UK.

Vivek Kapur (V)

Center for Infectious Disease Dynamics, Pennsylvania State University, University Park, PA, USA. vkapur@psu.edu.

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